Captivity and the co-diversification of great ape microbiomes.

Wild great apes harbor clades of gut bacteria that are restricted to each host species. Previous research shows the evolutionary relationships among several host-restricted clades mirror those of great-ape species. However, processes such as geographic separation, host-shift speciation, and host-filtering based on diet or gut physiology can generate host-restricted bacterial clades and mimic patterns of co-diversification across host species. To gain insight into the distribution of host-restricted taxa, we examine captive great apes living under conditions where sharing of bacterial strains is readily possible. Here, we show that increased sampling of wild and captive apes identifies additional host-restricted lineages whose relationships are not concordant with the host phylogeny. Moreover, the gut microbiomes of captive apes converge through the displacement of strains that are restricted to their wild conspecifics by human-restricted strains. We demonstrate that host-restricted and co-diversifying bacterial strains in wild apes lack persistence and fidelity in captive environments.

A great-ape view of the gut microbiome.

Humans assemble a specialized microbiome from a world teeming with diverse microorganisms. Comparison to the microbiomes of great apes provides a dimension that is indispensable to understanding how these microbial communities form, function and change. This evolutionary perspective exposes not only how human gut microbiomes have been shaped by our great-ape heritage but also the features that make humans unique, as exemplified by an expansive loss of bacterial and archaeal diversity and the identification of microbial lineages that have co-diversified with their hosts.

Rates of gut microbiome divergence in mammals.

The variation and taxonomic diversity among mammalian gut microbiomes raises several questions about the factors that contribute to the rates and patterns of change in these microbial communities. By comparing the microbiome compositions of 112 species representing 14 mammalian orders, we assessed how host and ecological factors contribute to microbiome diversification. Except in rare cases, the same bacterial phyla predominate in mammalian gut microbiomes, and there has been some convergence of microbiome compositions according to dietary category across all mammalians lineages except Chiropterans (bats), which possess high proportions of Proteobacteria and tend to be most similar to one another regardless of diet. At lower taxonomic ranks (families, genera, 97% OTUs), bacteria are more likely to be associated with a particular mammalian lineage than with a particular dietary category, resulting in a strong phylogenetic signal in the degree to which microbiomes diverge. Despite different physiologies, the gut microbiomes of several mammalian lineages have diverged at roughly the same rate over the past 75 million years; however, the gut microbiomes of Cetartiodactyla (ruminants, whales, hippopotami) have evolved much faster and those of Chiropterans much slower. Contrary to expectations, the number of dietary transitions within a lineage does not influence rates of microbiome divergence, but instead, some of the most dramatic changes are associated with the loss of bacterial taxa, such as those accompanying the transition from terrestrial to marine lifestyles and the evolution of hominids.

Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola.

Social bees collect carbohydrate-rich food to support their colonies, and yet, certain carbohydrates present in their diet or produced through the breakdown of pollen are toxic to bees. The gut microbiota of social bees is dominated by a few core bacterial species, including the Gram-negative species Gilliamella apicola We isolated 42 strains of G. apicola from guts of honey bees and bumble bees and sequenced their genomes. All of the G. apicola strains share high 16S rRNA gene similarity, but they vary extensively in gene repertoires related to carbohydrate metabolism. Predicted abilities to utilize different sugars were verified experimentally. Some strains can utilize mannose, arabinose, xylose, or rhamnose (monosaccharides that can cause toxicity in bees) as their sole carbon and energy source. All of the G. apicola strains possess a manO-associated mannose family phosphotransferase system; phylogenetic analyses suggest that this was acquired from Firmicutes through horizontal gene transfer. The metabolism of mannose is specifically dependent on the presence of mannose-6-phosphate isomerase (MPI). Neither growth rates nor the utilization of glucose and fructose are affected in the presence of mannose when the gene encoding MPI is absent from the genome, suggesting that mannose is not taken up by G. apicola strains which harbor the phosphotransferase system but do not encode the MPI. Given their ability to simultaneously utilize glucose, fructose, and mannose, as well as the ability of many strains to break down other potentially toxic carbohydrates, G. apicola bacteria may have key roles in improving dietary tolerances and maintaining the health of their bee hosts. IMPORTANCE: Bees are important pollinators of agricultural plants. Our study documents the ability of Gilliamella apicola, a dominant gut bacterium in honey bees and bumble bees, to utilize several sugars that are harmful to bee hosts. Using genome sequencing and growth assays, we found that the ability to metabolize certain toxic carbohydrates is directly correlated with the presence of their respective degradation pathways, indicating that metabolic potential can be accurately predicted from genomic data in these gut symbionts. Strains vary considerably in their range of utilizable carbohydrates, which likely reflects historical horizontal gene transfer and gene deletion events. Unlike their bee hosts, G. apicola bacteria are not detrimentally affected by growth on mannose-containing medium, even in strains that cannot metabolize this sugar. These results suggest that G. apicola may be an important player in modulating nutrition in the bee gut, with ultimate effects on host health.